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Comparative proteomic analysis of male and female plants in Jojoba (Simmondsia chinensis) leaves revealed changes in proteins involved in photosynthesis, metabolism, energy, and biotic and abiotic stresses

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Abstract

Jojoba is a dioecious shrub with female and male flowers in separated individuals. The plant native to North and Central American deserts, it’s cultivated in many other places worldwide for its valuable liquid wax. The male-biased ratio in cultivated jojoba affects the yield. To develop protein molecular markers for early gender differentiation, comparative proteomic study been conducted on male and female leaves. Using gel-based proteomic, 45 proteins were identified representing 19 different proteins with 18 known functions. The identified proteins were involved in photosynthesis, energy, metabolism and the respond to biotic and abiotic stress. Ribulose-1,5-bisphosphate carboxylase (Rubisco) and ATP synthase were the most abundant proteins in both male and female of jojoba leaves, both were upregulated in male compared to female. Both proteins have the potential to serve as protein biomarkers for early differentiation between male and female in jojoba plant. These results could help in better understanding the molecular mechanism of gender differentiation in jojoba.

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References

  • Agarwal M, Shrivastava N, Padh H (2011) Development of sex-linked AFLP markers in Simmondsia chinensis. Plant Breed 130:114–116

    Article  CAS  Google Scholar 

  • Agrawal V, Sharma K, Gupta S, Kumar R, Prasad M (2007) Identification of sex in Simmondsia chinensis (Jojoba) using RAPD markers. Plant Biotechnol Rep 1:207–210

    Article  Google Scholar 

  • Ainsworth C, Parker J, Buchanan-Wollaston V (1998) Sex determination in plants. Curr Top Dev Biol 38:167–223

    Article  CAS  PubMed  Google Scholar 

  • Al-Obaidi JR, Suliman BK, Al-Ani NK (2012) Molecular-based marker for sex differentiation of jojoba in vivo and in vitro Iraqi cultivars using RAPD-PCR technique. Sci Res Essays 7:522–527

    CAS  Google Scholar 

  • Al-Obaidi JR, Mohd-Yusuf Y, Chin-Chong T, Mhd-Noh N, Othman RY (2014) Differentially expressed plant defense protein EgPR10 And EgLTP genes in response to infection Of ganoderma in Elaeis guineensis (Oil Palm) seedlings. Pak J Agric Sci 51:731–742

    Google Scholar 

  • Al-Obaidi J, Saidi N, Usuldin S, Rahmad N, Zean NB, Idris A (2016) Differential proteomic study of oil palm leaves in response to in vitro inoculation with pathogenic and non-pathogenic ganoderma spp. J Plant Pathol 98:33–42

    Google Scholar 

  • Al-Soqeer A, Motawei MI, Al-Dakhil M, El-Mergawi R, Al-Khalifah N (2012) Genetic variation and chemical traits of selected new Jojoba (Simmondsia chinensis (Link) Schneider) genotypes. J Am Oil Chem Soc 89:1455–1461

    CAS  Google Scholar 

  • Amarger V, Mercier L (1995) Molecular analysis of RAPD DNA based markers: their potential use for the detection of genetic variability in jojoba (Simmondsia chinensis L Schneider). Biochimie 77:931–936

    Article  CAS  PubMed  Google Scholar 

  • Balmant KM, Parker J, Yoo M-J, Zhu N, Dufresne C, Chen S (2015) Redox proteomics of tomato in response to Pseudomonas syringae infection. Hortic Res 2:15043

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhardwaj M, Uppal S, Jain S, Kharb P, Dhillon R, Jain RK (2010) Comparative assessment of ISSR and RAPD marker assays for genetic diversity analysis in Jojoba [Simmondsia chinensis (Link) Schneider]. J Plant Biochem Biotechnol 19:255–258

    Article  Google Scholar 

  • Bita C, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    Google Scholar 

  • Bracale M et al (1991) Sex determination and differentiation in Asparagus officinalis L. Plant Sci 80:67–77

    Article  CAS  Google Scholar 

  • Chen F, Zhang S, Jiang H, Ma W, Korpelainen H, Li C (2011) Comparative proteomics analysis of salt response reveals sex-related photosynthetic inhibition by salinity in Populus cathayana cuttings. J Proteome Res 10:3944–3958

    Article  CAS  PubMed  Google Scholar 

  • Chen F, Zhang S, Zhu G, Korpelainen H, Li C (2013) Populus cathayana males are less affected than females by excess manganese: comparative proteomic and physiological analyses. Proteomics 13(16):2424–2437

    Article  CAS  PubMed  Google Scholar 

  • Correia O, Diaz Barradas MC (2000) Ecophysiological differences between male and female plants of Pistacia lentiscus L. Plant Ecol 149:131–142

    Article  Google Scholar 

  • Esfandiyari B, Davarynejad GH, Shahriari F, Kiani M, Mathe A (2012) Data to the sex determination in Pistacia species using molecular markers. Euphytica 185:227–231

    Article  CAS  Google Scholar 

  • Farooq MA, Ali B, Gill RA, Islam F, Cui P, Zhou W (2016) Chapter 2—breeding oil crops for sustainable production: heavy metal tolerance A2—Gupta, Surinder Kumar. Breeding oilseed crops for sustainable production. Academic Press, San Diego, pp 19–31

    Chapter  Google Scholar 

  • Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624

    Article  CAS  PubMed  Google Scholar 

  • Geisler DA et al (2012) Downregulation of the δ-subunit reduces mitochondrial ATP synthase levels, alters respiration, and restricts growth and gametophyte development in arabidopsis. Plant Cell 24:2792–2811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghazala A-S (2012) Proteomic responses of uninfected tissues of pea plants infected by root-knot nematode, fusarium and downy mildew pathogens. University of the West of England

  • Han Y, Wang L, Zhang X, Korpelainen H, Li C (2013) Sexual differences in photosynthetic activity, ultrastructure and phytoremediation potential of Populus cathayana exposed to lead and drought. Tree Physiol 33:1043–1060

    Article  CAS  PubMed  Google Scholar 

  • Heikrujam M, Sharma K, Kumar J, Agrawal V (2014) Generation and validation of unique male sex-specific sequence tagged sites (STS) marker from diverse genotypes of dioecious Jojoba-Simmondsia chinensis (Link) Schneider. Euphytica 199:363–372

    Article  Google Scholar 

  • Igamberdiev AU, Kleczkowski LA (2015) Optimization of ATP synthase function in mitochondria and chloroplasts via the adenylate kinase equilibrium. Front Plant Sci 6:10

    PubMed  PubMed Central  Google Scholar 

  • Ince AG, Karaca M, Onus AN (2010) A reliable gender diagnostic PCR assay for jojoba (Simmondsia chinensis (Link) Schneider). Genet Resour Crop Evol 57:773–779

    Article  CAS  Google Scholar 

  • Jangra S, Kharb P, Mitra C, Uppal S (2014) Early diagnosis of sex in Jojoba, Simmondsia chinensis (Link) Schneider by sequence characterized amplified region marker. Proc Natl Acad Sci India Sect B Biol Sci 84:251–255

    Article  Google Scholar 

  • Jorrín JV, Maldonado AM, Castillejo MA (2007) Plant proteome analysis: a 2006 update. Proteomics 7:2947–2962

    Article  PubMed  Google Scholar 

  • Jorrin-Novo JV (2014) Plant proteomics methods and protocols. In: Jorrin-Novo JV, Komatsu S, Weckwerth W, Wienkoop S (eds) Plant proteomics: methods and protocols. Humana Press, Totowa, pp 3–13

    Chapter  Google Scholar 

  • Juvany M, Munné-Bosch S (2015) Sex-related differences in stress tolerance in dioecious plants: a critical appraisal in a physiological context. J Exp Bot 66(20):6083–6092

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Mangal M, Dhawan AK, Singh N (2011) Assessment of genetic fidelity of micropropagated plants of Simmondsia chinensis (Link) Schneider using RAPD and ISSR markers. Acta Physiol Plant 33:2541–2545

    Article  CAS  Google Scholar 

  • Kumar S, Mangal M, Dhawan AK, Singh N (2012) Biotechnological advances in jojoba [Simmondsia chinensis (Link) Schneider]: recent developments and prospects for further research. Plant Biotechnol Rep 6:97–106

    Article  Google Scholar 

  • Li C, Xu G, Zang R, Korpelainen H, Berninger F (2007) Sex-related differences in leaf morphological and physiological responses in Hippophae rhamnoides along an altitudinal gradient. Tree Physiol 27:399–406

    Article  CAS  PubMed  Google Scholar 

  • Li T, Yun Z, Zhang D, Yang C, Zhu H, Jiang Y, Duan X (2015) Proteomic analysis of differentially expressed proteins involved in ethylene-induced chilling tolerance in harvested banana fruit. Front Plant Sci 6:845

    PubMed  PubMed Central  Google Scholar 

  • Nishiyama R et al (2000) Comparison of expressed sequence tags from male and female sexual organs of Marchantia polymorpha. DNA Res 7:165–174

    Article  CAS  PubMed  Google Scholar 

  • Rajangam AS, Gidda SK, Craddock C, Mullen RT, Dyer JM, Eastmond PJ (2013) Molecular characterization of the fatty alcohol oxidation pathway for wax-ester mobilization in germinated Jojoba seeds. Plant Physiol 161:72–80

    Article  CAS  PubMed  Google Scholar 

  • Reddy MP, Chikara J (2010) Biotechnology advances in Jojoba (Simmondsia chinensis). In: Ramawat KG (ed) Desert plants: biology and biotechnology. Springer, Berlin, pp 407–421

    Chapter  Google Scholar 

  • Reuss-Schmidt K, Rosenstiel TN, Rogers SR, Simpson AG, Eppley SM (2014) Effects of sex and Mycorrhizal fungi on gas exchange in the dioecious salt marsh grass Distichlis spicata. Int J Plant Sci 176:141–149

    Article  Google Scholar 

  • Sánchez M, Avhad MR, Marchetti JM, Martínez M, Aracil J (2016) Jojoba oil: a state of the art review and future prospects. Energy Convers Manag 129:293–304

    Article  Google Scholar 

  • Schulze J et al (2002) Malate plays a central role in plant nutrition. Plant Soil 247:133–139

    Article  CAS  Google Scholar 

  • Sharma K, Agrawal V, Gupta S, Kumar R, Prasad M (2008) ISSR marker-assisted selection of male and female plants in a promising dioecious crop: jojoba (Simmondsia chinensis). Plant Biotechnol Rep 2:239–243

    Article  Google Scholar 

  • Sharma R, Chowdhury VK, Jain S, Jain R (2009) A comparative study of genetic relationships among and within male and female genotypes of dioecious Jojoba (Simmondsia chinensis L. Schneider) using RAPD and ISSR markers. Asian J Hortic 4:184–193

    Google Scholar 

  • Sharma A, Zinta G, Rana S, Shirko P (2010) Molecular identification of sex in Hippophae rhamnoides L. using isozyme and RAPD markers. For Stud China 12:62–66

    Article  CAS  Google Scholar 

  • Sun Y et al (2014) Proteomics of Fusarium oxysporum race 1 and race 4 reveals enzymes involved in carbohydrate metabolism and ion transport that might play important roles in banana Fusarium wilt. PLoS One 9:e113818

    Article  PubMed  PubMed Central  Google Scholar 

  • Wegener KM et al (2008) High sensitivity proteomics assisted discovery of a novel operon involved in the assembly of photosystem II, a membrane protein complex. J Biol Chem 283:27829–27837

    Article  CAS  PubMed  Google Scholar 

  • Wiens D, Nickrent DL, Shaw CG, Hawksworth FG, Hennon PE, King EJ (1996) Embryonic and host-associated skewed adult sex ratios in dwarf mistletoe. Heredity 77:55–63

    Article  Google Scholar 

  • Xiong E, Wu X, Shi J, Wang X, Wang W (2013) Proteomic identification of differentially expressed proteins between male and female plants in Pistacia chinensis. PLoS One 8:e64276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong E, Wu X, Yang L, Wang W (2016) Proteomics in sex determination of dioecious plants. In: Hakeem KR, Tombuloğlu H, Tombuloğlu G (eds) Plant Omics: trends and applications. Springer International Publishing, Cham, pp 363–380

    Chapter  Google Scholar 

  • Xu X, Yang F, Yin C-Y, Li C-Y (2007) Research advances in sex-specific responses of dioecious plants to environmental stress. Chin J Appl Ecol 28:2626–2631

    Google Scholar 

  • Xu X, Peng G, Wu C, Korpelainen H, Li C (2008) Drought inhibits photosynthetic capacity more in females than in males of Populus cathayana. Tree Physiol 28:1751

    Article  PubMed  Google Scholar 

  • Xu P-L et al (2015) Proteomic analysis of sex conversion induced by CPPU in male grapevine of Vitis amurensis. VITIS J Grapevine Res 52:177

    Google Scholar 

  • Yang J, Fu Q (2012) The Preliminary analysis of specifi c protein on sex determination of Ginkgo biloba. L Sci Technol Inf 31:241

    Google Scholar 

  • Zhang S, Chen F, Peng S, Ma W, Korpelainen H, Li C (2010) Comparative physiological, ultrastructural and proteomic analyses reveal sexual differences in the responses of Populus cathayana under drought stress. Proteomics 10:2661–2677

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Feng L, Jiang H, Ma W, Korpelainen H, Li C (2012) Biochemical and proteomic analyses reveal that Populus cathayana males and females have different metabolic activities under chilling stress. J Proteome Res 11:5815–5826

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Liu H, Tao P, Chen H (2014a) Comparative proteomic analyses provide new insights into low phosphorus stress responses in maize leaves. PLoS One 9:e98215

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Jiang H, Zhao H, Korpelainen H, Li C (2014b) Sexually different physiological responses of Populus cathayana to nitrogen and phosphorus deficiencies. Tree Physiol 34:343–354

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Sun M, Zhang Q (2014c) Proteomic analysis of the heat stress response in leaves of two contrasting chrysanthemum varieties. Plant Omics 7:229

    Google Scholar 

  • Zhang S, Zhang Y, Cao Y, Lei Y, Jiang H (2016a) Quantitative proteomic analysis reveals Populus cathayana females are more sensitive and respond more sophisticatedly to iron deficiency than males. J Proteome Res 15:840–850

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Zhou R, Zhao H, Korpelainen H, Li C (2016b) iTRAQ-based quantitative proteomic analysis gives insight into sexually different metabolic processes of poplars under nitrogen and phosphorus deficiencies. Proteomics 16(4):614–628

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the service and training unit (STU), Agro-biotechnology Institute Malaysia (STU-ABI) for support, and Qassim University for providing jojoba samples.

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Authors and Affiliations

  1. Agro-Biotechnology Institute Malaysia (ABI), c/o MARDI Headquarters, 43400, Serdang, Selangor, Malaysia

    Jameel R. Al-Obaidi, Norasfaliza Rahmad & Nursyuhaida Mohd Hanafi

  2. Department of Biology, Faculty of Science and Art, Taibah University, Al-Ula, 43522, Saudi Arabia

    Mohammed Farouq Halabi

  3. Department of Plant Production and Protection, College of Agriculture and Veterinary Medicine, Al-Qassim University, Buraydah, 51452, Saudi Arabia

    Abdulrahman A. Al-Soqeer

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  1. Jameel R. Al-Obaidi
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  2. Norasfaliza Rahmad
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  3. Nursyuhaida Mohd Hanafi
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  4. Mohammed Farouq Halabi
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  5. Abdulrahman A. Al-Soqeer
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Correspondence to Jameel R. Al-Obaidi.

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Communicated by W. Wang.

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Al-Obaidi, J.R., Rahmad, N., Hanafi, N.M. et al. Comparative proteomic analysis of male and female plants in Jojoba (Simmondsia chinensis) leaves revealed changes in proteins involved in photosynthesis, metabolism, energy, and biotic and abiotic stresses. Acta Physiol Plant 39, 179 (2017). https://doi.org/10.1007/s11738-017-2485-7

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